Abstract
Understanding the nutritional requirements of Lytechinus variegatus is essential to define its role in the marine environment and necessary for successful culture of this species. Protein is an essential component for growth, yet the requirements for protein in most marine organisms are not known. Small Lytechinus variegatus (ca. 14 mm diameter, n=160) were collected at St. Joseph Bay, Florida in March 2000. They were held in aquaria and fed ad libitum one of four diets varying in protein concentration (9, 15, 21, or 33% dry weight) for 14 weeks. Diets ≥21% dry weight protein were sufficient for maximal growth and survivorship. Individuals fed a diet low in protein compensated by consuming higher quantities of food per gram wet weight. However, the protein was insufficient to support maximal growth and survivorship. Total dry matter absorption, protein absorption, and carbohydrate absorption of the prepared feeds were higher than reported for natural diets. Total production and production efficiency was lowest in those fed the low-protein diet. Gonad production occurred in individuals with test diameters smaller than reported previously in field populations and was lowest in those fed the low-protein diet. The acini of both females and males were predominantly composed of nutritive phagocytes, suggesting that growing L. variegatus use the gonad primarily as a nutrient storage organ and not for reproduction. In females the growth rate of oocytes increased with dietary protein. In males, protein concentration ≥21% resulted in an increase in the volume of germinal epithelium and a decrease in the volume of nutritive phagocytes. The minimal requirement for protein in L. variegatus from approximately 1 g to 15 g total weight is >15% dry weight for the conditions of this experiment. The requirement for a diet >15% protein corroborates with field studies that indicate L. variegatus consumes epibionts and animal tissues preferentially to seagrass, and that the microbial, microfloral, and microfaunal community living on the seagrass may provide the extra protein required for growth and survival of small L. variegatus.
Similar content being viewed by others
References
Akiyama DM, Dominy WG, Lawrence AL (1992) Panaeid shrimp nutrition. In: Fast AW, Lester LJ (eds) Culture of marine shrimp: principles and practices. Elsevier, Amsterdam, pp 539–572
Akiyama T, Unuma T, Yamamoto T (2001) Optimum protein level in a purified diet for young red sea urchin Pseudocentrotus depressus. Fish Sci 67:361–363
Beddingfield SD, McClintock JB (1998) Differential survivorship, reproduction, growth and nutrient allocation in the regular echinoid Lytechinus variegatus (Lamarck) fed natural diets. J Exp Mar Biol Ecol 226:195–215
Beddingfield SD, McClintock JB (2000) Demographic characteristics of Lytechinus variegatus (Echinoidea: Echinodermata) from three habitats in a north Florida Bay, Gulf of Mexico. Mar Ecol 21:17–40
Briscoe CS, Sebens KP (1988) Omnivory in Strongylocentrotus droebachiensis (Muller) (Echinodermata: Echinoidea): predation on subtidal mussels. J Exp Mar Biol Ecol 115:1–24
Burkholder PR, Burkholder LM, Rivero JA (1959) Some chemical constituents of turtle grass, Thalassia testudinum. Bull Torrey Bot Club 86:88–93
Byrne M (1990) Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and a sheltered subtidal habitat on the west coast of Ireland. Mar Biol 104:275–289
Caltagirone A, Francour P, Fernandez C (1992) Formulation of an artificial diet for rearing of the sea urchin Paracentrotus lividus I. Comparison of different binding agents. In: Scalera-Liaci L, Canicatti C (eds) Echinoderm research. Balkema, Rotterdam, pp 115–119
Cantor AB (1997) Extending SAS survival analysis techniques for medical research. SAS Institute, Cary, N.C.
Dawes CJ, Lawrence JM (1983) Proximate composition and caloric content of seagrasses. Mar Technol Soc J 17:53–58
de Jong-Westman M, March BE, Carefoot TH (1995) The effect of different nutrient formulations in artificial diets on gonad growth in the sea urchin Strongylocentrotus droebachiensis. Can J Zool 73:1495–1502
De Ridder C, Lawrence JM (1982) Food and feeding mechanisms: Echinoidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema, Rotterdam, pp 57–115
Dubois M, Gilles KA, Gilles JK, Hamilton JK, Rebers PA, Smith R (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Elmhirst R (1922) Habits of Echinus esculentus. Nature 110:667
Emson RH, Moore PG (1998) Diet and gonad size in three populations of Echinus esculentus. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Balkema, Rotterdam, pp 641–644
Engstrom NA (1982) Immigration as a factor in maintaining populations of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea) in seagrass beds on the southwest coast of Puerto Rico. Stud Neotrop Fauna Environ 17:51–60
Fernandez C, Boudouresque C (1998) Evaluating artificial diets for small Paracentrotus lividus (Echinodermata: Echinoidea). In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Balkema, Rotterdam, pp 651–656
Fernandez C, Dombrowski E, Caltagirone A (1995) Gonadic growth of adult sea urchins, Paracentrotus lividus (Echinodermata: Echinoidea) in rearing: the effect of different diet types. In: Emson R, Smith A, Campbell A (eds) Echinoderm research. Balkema, Rotterdam, pp 269–275
Fuji A (1967) Ecological studies on the growth and food consumption of Japanese common littoral sea urchin, Strongylocentrotus intermedius (A. Agassiz). Mem Fac Fish Hokkaido Univ 15:83–160
George SB, Lawrence JM, Lawrence AL, Ford J (2000) Fertilization and development of eggs of the sea urchin Lytechinus variegatus maintained on extruded feed. J World Aquacult Soc 31:232–238
Giese AC (1966) On the biochemical constitution of some echinoderms. In: Boolootian RA (ed) Physiology of Echinodermata. Interscience, New York, pp 757–796
Greenway M (1995) Trophic relationships of macrofauna within a Jamaican seagrass meadow and the role of the echinoid Lytechinus variegatus (Lamarck). Bull Mar Sci 56:719–736
Grosjean P, Spirlet C, Jangoux M (1996) Experimental study of growth in the echinoid Paracentrotus lividus (Lamarck, 1816) (Echinodermata). J Exp Mar Biol Ecol 201:173–184
Hammer HS, Watts SA, Lawrence JM, Lawrence AL, McClintock JB (2001) The effect of dietary protein concentration on gonad composition and gametic condition in the sea urchin Lytechinus variegatus. Am Zool 49:1042–1043
Herrera JC (1998) Nutritional strategies of echinoplutei. PhD thesis, University of Florida, Gainesville
Hinegardner RT (1969) Growth and development of the laboratory cultured sea urchin. Biol Bull 137:465–475
Jensen M (1969) Breeding and growth of Psammechinus miliaris. Ophelia 7:65–78
Kawamura K (1974) Fishery biological studies on a sea urchin, Strongylocentrotus intermedius (A. Agassiz). Sci Rep Hokkaido Fish Exp Station 16:1–54
Kelly MS, Brodie CC, McKenzie JD (1998) Somatic and gonadal growth of the sea urchin Psammechinus miliaris (Gmelin) maintained in polyculture with the Atlantic salmon. J Shellfish Res 17:1557–1562
Klinger TS (1982) Feeding rates of Lytechinus variegatus Lamarck (Echinodermata: Echinoidea) on differing physiognomies of an artificial food of uniform composition. In: Lawrence JM (ed) Echinoderms: proceedings of the international conference, Tampa Bay. Balkema, Rotterdam, pp 29–32
Klinger TS, Lawrence JM, Lawrence AL (1997) Gonad and somatic production of Strongylocentrotus droebachiensis fed manufactured feeds. Bull Aquacult Assoc Can 1:35–37
Klinger TS, Lawrence JM, Lawrence AL (1998) Digestion, absorption, and assimilation of prepared feeds by echinoids. In: Mooi R, Telford M (eds) Echinoderms: San Francisco. Balkema, Rotterdam, pp 713–721
Lawrence JM (1975) On the relationship between marine plants and sea urchins. Oceanogr Mar Biol Annu Rev 13:213–286
Lawrence JM (2000) Conflict between somatic and gonadal growth in sea urchins: a review. Workshop on coordination of green sea urchin research in Atlantic Canada, Moncton. http://crdpm.umcs.ca/OURSIN/
Lawrence JM, Olave S, Otaiza R, Lawrence AL, Bustos E (1997) Enhancement of gonad production in the sea urchin Loxechinus albus in Chile fed extruded feeds. J World Aquacult Soc 28:91–96
Leighton DL (1968) A comparative study of food selection and nutrition in the abalone, Haliotis rufescens Swainson, and the sea urchin, Strongylocentrotus purpuratus Stimpson. PhD thesis, University of California, San Diego
Levin VS, Naidenko VP (1987) Artificial diets for the laboratory-maintained sea urchin Strongylocentrotus intermedius. Mar Biol (Vladivostok) 6:50–56
Lowe EF (1975) Absorption efficiencies, feeding rates, and food preferences of Lytechinus variegatus (Echinodermata: Echinoidea) for selected marine plants. PhD thesis, University of South Florida, Tampa
Lowe EF, Lawrence JM (1976) Absorption efficiencies of Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea) for selected marine plants. J Exp Mar Biol Ecol 21:223–234
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin reagent. J Biol Chem 1934:265–275
Mazur JE, Miller JW (1971) A description of the complete metamorphosis of the sea urchin Lytechinus variegatus cultured in synthetic sea water. Ohio J Sci 71:30–36
McBride SC, Lawrence JM, Lawrence AL, Mulligan TJ (1998) The effect of protein concentration in prepared feeds on growth, feeding rate, total organic absorption, and gross assimilation efficiency of the sea urchin Strongylocentrotus fransiscanus. J Shellfish Res 17:1563–1570
McClintock JB, Klinger TS, Lawrence JM (1982) Feeding preferences of echinoids for plant and animal food models. Bull Mar Sci 32:365–369
McEdward LR, Herrera JC (1999) Body form and skeletal morphometrics during larval development of the sea urchin Lytechinus variegatus Lamarck. J Exp Mar Biol Ecol 232:151–176
Meidel SK, Scheibling RE (1999) Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 134:155–166
Moir RJ (1994) The ‘carnivorous’ herbivore. In: Chivers DJ, Langer P (eds) The digestive system in mammals: food, form and function. Cambridge University Press, New York pp 87–102
Moore HB, McPherson BF (1965) A contribution to the study of the productivity of the urchins Tripneustes esculentus and Lytechinus variegatus. B Mar Sci 15:855–870
Moore HB, Jutare T, Bauer JC, Jones JA (1963) The biology of Lytechinus variegatus. Bull Mar Sci Gulf Carib 13:23–53
Olave S, Bustos E, Lawrence JM, Carcama P (2001) The effect of size and diet on gonad production by the Chilean sea urchin Loxechinus albus. J World Aquacult Soc 32:210–214
Pawson DL, Miller JE (1982) Studies of genetically controlled phenotypic characters in laboratory-reared Lytechinus variegatus (Lamarck) (Echinodermata: Echinoidea) from Bermuda and Florida. In: Lawrence JM (ed) Echinoderms: proceedings of the international conference, Tampa Bay. Balkema, Rotterdam, pp 165–171
Regis M-B (1981) Aspects morphometriques de la croissance de deux Echinoides du Golfe de Marseille, Paracentrotus lividus (Lmk) et Arbacia lixula L. Cah Biol Mar 22:349–370
Rivera JA (1979) Aspects of the biology of Lytechinus variegatus (Lamarck, 1816) at Jobos Bay, Puerto Rico (Echinoidea: Toxopneustidae). Master’s thesis, University of Puerto Rico, Mayaguez
Robinson SMC, Colborne L (1997) Enhancing roe of the green sea urchin using an artificial food source. Bull Aquacult Assoc Can 97:14–20
Russell MP (1998) Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus droebachiensis (Muller). J Exp Mar Biol Ecol 220:1–14
Sklener SA (1994) Interactions between sea urchin grazers (Lytechinus variegatus and Arbacia punctulata) and mussels (Modiolus americanus): a mutualistic relationship? Master’s thesis, University of South Alabama, Mobile
Spirlet C, Grosjean P, Jangoux M (1994) Differentiation of the genital apparatus in a juvenile echinoid (Paracentrotus lividus). In: David B, Guille A, Feral J, Roux M (eds) Echinoderms through time. Balkema, Rotterdam, pp 881–886
Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern Pacific coast. University of Washington Press, Seattle
Traer K (1980) The consumption of Posidonia oceanica Delile by echinoids at the Isle of Ischia. In: Jangoux M (ed) Echinoderms: present and past. Balkema, Rotterdam, pp 241–244
Vadas RL, Fenchel T, Ogden JC (1982) Ecological studies on the sea urchin, Lytechinus variegatus, and the algal-seagrass communities of the Miskito Cays, Nicaragua. Aquat Bot 14:109–125
Wallace BD (2001) The effects of dietary protein concentration on feeding and growth of small Lytechinus variegatus. Master’s thesis, University of Alabama at Birmingham
Watts SA, McClintock JB, Lawrence JB (2001) The ecology of Lytechinus variegatus. In: Lawrence JM (ed) The biology of edible sea urchins. Elsevier, Amsterdam, pp 375–393
Wilson RP (1989) Amino acids and proteins. In: Halver JE (ed) Fish nutrition. Academic, San Diego, pp 112–151
Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River, N.J.
Acknowledgements
The authors would like to thank Dr. Mickie Powell, Scott Hofer, Adele Cunningham, Victoria Gibbs, Rebecca Worrell, and Janna Owens for technical assistance and animal care. This research was supported by the Mississippi–Alabama Sea Grant Consortium, grant number NA86RG0039, and the Alabama Academy of Science. This research was approved by the Animal Resource Program (011103710) at the University of Alabama at Birmingham.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P.W. Sammarco, Chauvin
Rights and permissions
About this article
Cite this article
Hammer, B.W., Hammer, H.S., Watts, S.A. et al. The effects of dietary protein concentration on feeding and growth of small Lytechinus variegatus (Echinodermata: Echinoidea). Marine Biology 145, 1143–1157 (2004). https://doi.org/10.1007/s00227-004-1391-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-004-1391-x